S u r v e i ll a n c e a n d o u t b r e a k r e p o r t s
Chang es i n preve ntion an d outbreak manag e m e nt of
Leg ion nai res’ disease i n th e neth e rLan ds betwe e n
two Large outbreaks in 1999 and 2006
G J Sonder (email@example.com)1, J A van den Hoek1, L P Bovée1, F E Aanhane1, J Worp1, M Du Ry van Beest Holle2,
J E van Steenbergen2, J W den Boer3, E P Ijzerman3, R A Coutinho2
1. Gemeentelijke Gezondheidsdienst (GGD) Amsterdam (Public Health Service Amsterdam) Department of Infectious Diseases,
Amsterdam, the Netherlands
2. Centrum Infectieziektebestrijding (Centre for Infectious Disease Control, CIb), Rijksinstituut voor Volksgezondheid en Milieu
(National Institute for Public Health and the Environment, RIVM), Preparedness and Response Unit, Bilthoven, the Netherlands
3. Regional Laboratory of Public Health Haarlem, Haarlem, the Netherlands
We describe an outbreak of Legionnaires’ disease in 2006 in
Amsterdam, the Netherlands. Comparisons with the outbreak that Here we describe the second large outbreak of LD in the
took place in 1999 are made to evaluate changes in legionella Netherlands in 2006, and evaluate the effectiveness of changes
prevention and outbreak management. The 2006 outbreak was in legislation, prevention management and outbreak management
caused by a wet cooling tower. Thirty-one patients were reported. implemented after the first large outbreaks in 1999.
The outbreak was detected two days after the first patient was
admitted to hospital, and the source was eliminated five days Methods
later. The 1999 outbreak was caused by a whirlpool at a flower In the Netherlands, LD has been a reportable disease since
show, and 188 patients were reported. This outbreak was detected 1987. Every diagnosed case has to be reported to the local Public
14 days after the first patient was admitted to hospital, and two Health Service (PHS), and is registered nationally by the Centre
days later the source was traced. Since 1999, the awareness of for Infectious Disease Control (CIb). Since 2002, the local PHSs
legionellosis among physicians, the availability of a urinary antigen report to CIb by the internet.
tests and more efficient early warning and communication systems
improved the efficiency of legionellosis outbreak management. For A confirmed LD case is a patient with pneumonia, confirmed
prevention, extensive legislation with clear responsibilities has by a positive laboratory test (urinary antigen test, positive culture,
been put in place. For wet cooling towers, however, legislation positive polymerase chain reaction (PCR), positive IgM antibody or
regarding responsibility and supervision of maintenance needs to a significant increase in IgG antibody ELISA test). After a case of
be improved. LD has been reported to the PHS, patient information is gathered
including demographics, diagnosis, underlying disease, domestic
Introduction risk factors, risk factors at work, travel, and leisure activities in the
Legionnaires’ disease (LD) is an acute pneumonia caused by 21 days before onset of disease, using a standardised questionnaire
infection with bacteria of the genus Legionella. Inhalation of .
aerosolized water containing the bacteria is the primary mode
of acquisition. Although cases of LD are often sporadic, large Any unusual number of reported cases in time or place will lead
outbreaks can be caused by communal sources, such as ‘hot tubs’ to an outbreak investigation as to a common source. In case an
or ‘spa pools’ [1,2] and hospital or hotel showers [3,4]. Wet cooling outbreak is suspected, depending on the suspected source, active
towers can emit contaminated aerosols, with dispersal over long case-finding is initiated by the PHS in order to detect and eliminate
distances, sometimes causing major outbreaks [5-15]. the source as soon as possible. Depending on the magnitude
of the outbreak, active case-finding comprises alerting general
In the Netherlands, the first large LD outbreak occurred in practitioners and hospitals in the PHS area, other PHS branches
1999; it affected 188 patients of whom 23 died. This epidemic and international early warning systems. Since 2002, in case an
was caused by aerosol transmission from a display whirlpool at outbreak is suspected that is not confined to one PHS area, the
a flower show, and was not recognized as an LD outbreak until CIb informs the other PHSs and other physicians by email service,
14 days after the first patient was diagnosed with pneumonia of which makes it possible to notify them instantly. The public can
unknown origin. The source was identified within a week after the be warned by local or national press and television.
epidemic was detected as an LD outbreak; 10 days after the show
had ended, when already 71 patients had been admitted to various To strengthen local efforts to identify sources, a specialized team
hospitals throughout the country. The 1999 outbreak was evaluated from the Regional Public Health Laboratory of Haarlem has offered
extensively  and this has led to changes in prevention policies, sampling services to all public health services in the Netherlands
legislation and outbreak management strategies. since 2002, and serves as a reference laboratory where both human
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and environmental strains are genotyped. The laboratory keeps a general practitioners who were on call that weekend (8 and 9 July).
national register of sampled potential sources. All six Amsterdam hospitals were called to alert and inform the
microbiologists about the outbreak. Also, all other PHS branches in
For the 2006 outbreak investigation, the following case the Netherlands were notified by CIb email service and requested
definition was made: confirmed cases were patients with clinical to report any unusual number of LD cases or cases that could
signs of pneumonia, with fever > 380C, cough and shortness of be related to a recent visit to Amsterdam. During the weekend,
breath, who had been to the eastern part of Amsterdam (with zip nine additional cases were reported. Extensive interviewing did
codes 1011 and 1018) between 8 June and 11 July and with a not suggest a common source for these infections. None of the
confirmed laboratory test (positive urinary antigen test; positive patients had traveled recently. The majority of patients were living
culture; fourfold increase in antibody titer or seroconversion in a in the city centre, in an area about 500 meters east of the central
paired sample). railway station with zip codes 1011 or 1018, which is an area with
a 2,5-3 km in diameter. Most of these patients reported onset of
All hospital laboratories were asked to send available cultures disease on the first of July (Figure 1).
to the reference laboratory in Haarlem for genotyping, where
Amplified Fragment Length Polymorphism (AFLP) was used for On 8 July, the first sample was taken from a possible source, a
DNA fingerprinting. newly installed display fountain, because most patients reported by
then were living in the fountain area. This fountain was immediately
Although wet cooling towers are a common source of LD closed.
outbreaks, in the Netherlands registration of these towers is not
addressed in the law (Table 1). As soon as a cooling tower was Because it was possible that the outbreak was not confined
suspected as the source of the outbreak, for tracing of this source to Amsterdam, on Monday 10 July, a national outbreak team
wind directions were used as published by the Dutch National was established, with participants from the PHS Amsterdam,
Meteorological Institute KNMI. [www.knmi.nl/klimatologie/ the CIb and the Public Health Laboratory of Haarlem. The CIb
daggegevens/index.cgi] All environmental samples were obtained started enhanced national active case-finding by contacting all
by the department of Infectious Diseases of the PHS Amsterdam infectious disease control physicians at PHS facilities in the
in cooperation with the Public Health Laboratory Haarlem regions surrounding Amsterdam. They were asked to telephone all
hospitals in their region and ask if there had been any LD patients
Results admitted. Also on 10 July, all general practitioners, microbiologists
Source tracing and infectiologists in Amsterdam were alerted by post. In order
On Thursday 6 July 2006, three cases of LD were reported to to alert as many people in the Netherlands as possible, a press
the PHS in Amsterdam, all diagnosed on the same day by a urine release was issued on Monday announcing the unusual number of
test indicating type I infection. On Friday 7 July, the second day LD patients in Amsterdam.
when five cases were reported, the PHS Amsterdam continued
the source tracing and started active case-finding by emailing all
Ta b l e 1
Legislation and supervision of preventive legionella source cleansing in the Netherlands, 2007
Laws Supervisor Location Object/source
Law on drinking water Chapter IIIC Inspectorate of VROM Hospitals, housing, camping Drinking water installations
sites, asylum seekers’
Chapter IIIC articles 17j, 17o, Inspectorate of VROM Drinking water companies Drinking water delivery
17p, 17q (waterworks)
Law on occupational health Policy regulation* document Labor Inspectorate Locations in companies with Cooling towers
and safety 4.87-1 SZW exposure risk for employees Humidifiers
Food and Consumer product Locations in companies with installations**
safety authority public exposure risk
Labor Inspectorate Inland shipping Drinking water installations
Inspectorate of Transport, Ocean shipping Industrial water
Public Works and Water installations
Inspectorate of Transport, Airplanes
Public Works and Water
Law on hygiene and safety Articles 2a-2d Provinces Public baths and swimming Swimming and bathing water
public baths and swimming pools
Law on collective prevention Municipalities Large-scale events All atomizing installations
in public health
VROM: Ministry of Housing, Spatial planning and the Environment
SZW: Ministry of Social Affairs and Employment
* A policy regulation is not a law but a guideline; it describes best practice but does not have to be obeyed.
** Atomizing installations outside companies (such as fountains on squares or in shopping malls) are not part of this, or any other law.
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In the ten days preceding the outbreak, the wind appeared to He fell ill on 4 July and refused admittance to hospital for further
be mainly west and north-west (Figure 1). Therefore, the team testing. A post-mortem lung specimen was tested and legionella
started to look for fountains and wet cooling towers north-west of bacteria could be detected by DNA isolation.
the affected area. Subsequently a second display fountain in this
area was sampled and immediately closed. Since registration of In July, many tourists visit Amsterdam. Because the LD source
wet cooling towers is not mandatory, a register of these cooling was so close to Amsterdam Central Station, the fear arose that
towers was not available. However, in 2003, a list of wet cooling international visitors could have been exposed, perhaps in large
towers was made in Amsterdam for a study on the prevalence of numbers. Therefore, on 12 July, the European Surveillance Scheme
legionellae, but had not since been updated. With the help of for Travel-Associated Legionnaires’ Disease issued a community
Google Earth, we looked for new, not registered cooling towers, cluster alert to its participants  and a preliminary report was
and also inspected the area. As a result, every cooling tower in the published in Eurosurveillance . On 13 July, information on the
outbreak area was inspected and sampled. At the end of the day on outbreak appeared in ProMed . No cases in tourists or visitors
10 July, we detected one (previously not listed) wet cooling tower to Amsterdam were reported.
on ground floor level, a few meters east of a construction site just
east of the central station. This cooling tower was installed on 10 Characteristics of patients
June and was visibly not well maintained. Samples were taken from In total, 31 patients with LD were reported in this outbreak:
the tower and as a precautionary measure the tower was closed as their characteristics are shown in Table 2. Seventy-four percent
soon as possible in the early morning of Tuesday 11 July. The next were men, and the case fatality rate was 10%. Sixty-five percent
day, the laboratory results showed positive culture and revealed reported possible risk factors associated with developing LD.
a concentration of 5 million colony-forming units per liter. In a
follow-up press release issued on the same day, it was announced Cultures and DNA fingerprinting
that most patients affected lived in or had recently visited the area From seven patients epidemiologically linked to the contaminated
east of Amsterdam Central Station, and that a cooling tower in this cooling tower, cultures were available for DNA fingerprinting,
area was the probable source of the outbreak. enabling comparison with the bacteria obtained from the cooling
tower. All seven matched. In Figure 3, three of these seven samples
Active case-finding are shown (patient 2, 3 and 4) in comparison to another patient not
On 10 July, all public health physicians in the country were related to this outbreak (patient 1) and samples from the cooling
updated about the outbreak by CIb email service and asked to tower (samples 5,6,7 and 8). At the same time, at a routine control,
query all LD patients about visits to Amsterdam, including specific legionellae were found in another wet cooling tower in Amsterdam,
locations visited. In total, active case-finding yielded seven LD five kilometers south-west of Central Station. However, the strain
patients who lived outside Amsterdam but all of them worked in found in this tower (samples 9 and 10) was evidently different from
or very near the construction site adjacent to the questionable the strain found in the outbreak patients.
cooling tower. These findings confirmed our suspicion that it was
the source of the outbreak. Discussion
Active case finding within the Occupational Health Services of The most important development since the 1999 outbreak is that
the construction companies working near the cooling tower revealed urinary antigen tests have become widely available and physicians
that one construction worker had died on 6 July from pneumonia. more aware of LD. The 1999 outbreak was not recognized as an
Legionnaires’ Disease (LD) patients in Amsterdam linked to a cooling tower, by date of onset of disease, June – July 2006 (n=31)
10 1st LD case reported 30
Cooling tower M installed
Temperature (C) Wind velocity (m/s)
9 Fountain N off
Fountain N installed 25
Cooling tower M off
Number of patients
6 Works in Amsterdam
5 Since 28 June in NL Lives in Amsterdam 15
4 Wind velocity (m/s)
Average temperature 10
Date and wind direction
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LD outbreak until 14 days after the first patient was hospitalized whirlpool, and sampling revealed abundant legionella growth six
and diagnosed as a case of pneumonia of unknown origin. Hospital weeks after the outbreak was recognized. 
physicians were not aware that LD was a notifiable disease; they
contacted the PHS because of the unusual number of pneumonia Until 2002, national registration of reported LD cases was
patients. In 2006, the first patient was diagnosed with LD within done by post from PHSs to CIb, where cases were subsequently
two days after hospital admission and reported to the PHS the same entered in a database. This procedure resulted in delays in the
day the diagnosis was confirmed. ‘early warning system’. Since 2002, national registration is done
by internet reporting, which is much faster. Especially outbreaks in
In the Amsterdam outbreak in which standardized questionnaires different PHS districts can now be detected faster than in 1999.
were used, the likelihood of a source outside a building (i.e. a cooling Also, communication from the CIb to PHSs has improved by the
tower or a fountain) became clear after two days, by exclusion of installation of a CIb email service in 2002. The service makes it
communal sources. The actual source, a cooling tower, was located possible to notify public health and other physicians instantly. In
within four days after the first patient was diagnosed. In contrast, 1999, this was done by telephone and facsimile, which was much
in 1999, a case control-study showed that it was likely that the slower. Also, internationally, early warning systems have been put
source of the outbreak was situated at a flower show. Subsequent in place. [28,20]
environmental risk assessment led to the most likely source, a
The work of the reference laboratory has also proven successful;
in the first two years of the project, the lab discovered 17 LD
clusters, 12 of which would not have been identified in a timely
manner without this outbreak detection program.  Because the
Ta b l e 2
Characteristics of patients with Legionnaires’ disease associated
with cooling tower as most likely source of infection, Amsterdam,
June – July 2006 (n=31) Figure 2
The annual number of reported cases of Legionnaires’ disease in
Total number of patients 31 100% The Netherlands, 1987-2006
Outbreak 1999 Outbreak 2006
Flower show Cooling tower
Male 23 74% 188 patients 31 patients
Number of reported cases
Female 8 26% 500
Average age (range) in years 56 (32-81)
Age distribution in years
30-39 3 10% 0
40-49 8 26%
50-59 7 23%
60-69 9 29%
70-79 3 10%
80-89 1 3% Results of DNA fingerprinting of four Legionnaires’ disease patients
and two cooling towers in Amsterdam, 2006
Urinary test 31 100%
er am 3*
sa le 2
ol tow 1 s ple
rk ow 2 sa le
Co g er 1 p
Urinary test + culture 7 23%
ow 1 s
History taken in acute stage
Co g er
Patient 17 55%
Co g t
Ma g t
Pa nt 1
Pa t 2
Pa t 3
Co nt 4
Relative/proxy 14 45%
Number of deaths, case fatality rate 3 10%
Diabetes type II 5 16%
Immune deficiency 2 6%
COPD 3 10%
Other lung disease 1 3%
Hypertension 2 6%
Smoker 11 35%
Alcoholism 2 6%
* Patients and cooling tower 1 match
Any associated factor 20 65% $ cooling tower 2 was located 5 kilometers south-west of cooling tower 1
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project was so successful, it was implemented in routine outbreak must report LD patients to the local PHS within 24 hours of the
control and is coordinated by CIb since 2006.  diagnosis after which source tracing and elimination can take place
as described above in the ‘Methods’ section .
Because of their experience with sampling of possible legionella
sources, in the 2006 outbreak the Regional Public Health Next steps
Laboratory of Haarlem could take the first samples of suspected Although the Ministry of Social Affairs and Employment is
sources immediately after they were identified, starting on Saturday responsible for legionella control in wet cooling towers, their actual
evening. Four days after the first patient was diagnosed, the actual supervision, so far, is limited. Registration of these towers is not
source was sampled and one day later closed. addressed in the law but in a policy regulation, which is a guideline
that describes ‘best practice’. In response to the Amsterdam
Increased awareness and availability of antigen tests are probably outbreak, the minister of Social Affairs and Employment stated
the reason why since the 1999 outbreak, the number of reported that the responsibility for registration of cooling towers lay with
LD cases in the Netherlands has increased steadily (Figure 2). In the municipalities, and that voluntary registration was expected
2006, the incidence of LD in the Netherlands was higher than to be sufficient.
in previous years. This increase cannot be explained only by the
Amsterdam outbreak or increased awareness. The same trend was As for drinking water, it is urgently needed that wet cooling
seen in the United Kingdom.  In both countries many sporadic towers are sampled at regular intervals, and that these cooling
cases spread all over the country were reported, which may be towers, together with their test results, are registered nationally.
associated with certain weather conditions. In a recent study, warm Positive cultures should be fingerprinted and the results entered in
and wet weather patterns, but not the hottest ones, were found to the national database. This way, prevention will improve because
be associated with a higher incidence of LD in The Netherlands maintenance will be monitored, and matches with patients’ cultures
between 2003 and 2007  can be made as soon as possible.
Legionella prevention and legislation In 2007, a register of wet cooling towers was still not in place.
After the 1999 outbreak, the Dutch government launched a plan In 2003, 30 wet cooling towers were registered in Amsterdam as
to combat Legionnaires’ disease  which has resulted in the part of a study. During the 2006 outbreak 14 new wet cooling
report ‘Controlling Legionnaires’ Disease’, published by the Health towers were found. Although registration of cooling towers is not
Council in 2003 . The report targets four areas in which the officially their task, in the beginning of the summer of 2007, the
risk of infection could be reduced at acceptable cost: 1) European- PHS Amsterdam decided to make a start with an updated list of wet
wide agreement on guidelines (since about half of the patients are cooling towers. At the end of the summer, 73 of such cooling towers
infected abroad); 2) rapid diagnosis and treatment; 3) modification were registered, more than twice as many as in 2003. Possibly,
of water fittings and implementation of management plans; and 4) with a larger database that also includes cooling tower test results,
stimulation of research to further rationalize prevention policies. The more sources of such outbreaks as described in this paper can be
report states that some water atomizers (those used at large scale found and prevented or eliminated faster in the future.
events, by residential properties, by small companies, and atomizers
that are not connected to the main water system), and wet cooling
towers used for comfort cooling need better maintenance. A ck now led gem e nts
The authors would like to thank public health nurses of the Public
New preventive legislation about control of legionella in water Health Service department of infectious diseases for collecting and
has been put in place, with clear responsibilities. In March 2005, documenting all data and Jacob Bruin for sampling potential sources
the Ministry of Housing, Spatial Planning and the Environment during the outbreak.
(VROM) published a summary on the prevention and the legislation
concerning the control of legionella in water. LD prevention is
divided into pro-active and reactive source cleansing. For preventive
pro-active cleansing, four laws are in place that apply to different
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